virus resistence

001_JPP_Review_15321-07-2008 9:57 Pagina 153 Journal of Plant Pathology (2008), 90 (2), 153-171 Edizioni ETS Pisa, 2008 153 INVITED REVIEW PLANT RESISTANCE RESPONSES TO VIRUSES P. Palukaitis1 and J.P. Carr2 1 Scottish 2 Department Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK SUMMARY Plants have developed numerous approaches to resist infection by viruses. On the other hand, in many instances viruses have evolved to overcome these various resistance responses and barriers. The extent to which viruses can overcome some or all of these responses and barriers determines the extent to which they are able to colonize plants of a given genotype or species. Resistance against plant viruses occurs at different levels and by various mechanisms, most of which largely remain uncharacterized. Here, we will consider these various levels of resistance, as well as the types of resistance responses, the isolated genes involved in resistance, the signalling pathways that have been described, and the various resistance factors that have been implicated in resistance to specific viruses. cells. With one exception, these are still the major forms of resistance that occur against virus infection (rev. by Bruening, 2006). Besides these various levels described below, resistance also occurs via the surveillance mechanism designated RNA silencing or RNA inhibition (RNAi). We will not consider RNAi in detail here, as it has been covered in many reviews in recent years (Brodersen and Voinnet, 2006; Burgyán, 2006; Li and Ding, 2006; Vaucheret, 2006; Ding and Voinnet, 2007). Nevertheless, the effects of RNAi may also be a contributing factor to either the various types of induced resistance or the barriers to infection described below. TYPES OF RESISTANCE INTRODUCTION Francis Holmes (1946) made some poignant observations concerning the types of resistance plants have to viruses, when he examined the host range of Tobacco etch virus (TEV) and Tobacco mosaic virus (TMV) and showed that (besides whether or not the plants showed local or systemic symptoms) the plant’s responses could be divided into four categories (Table 1). He found that many plant species did not show detectable virus multiplication in the inoculated leaves, while other species did; however, there was also differentiation amongst the latter group as to whether the plant species become infected systemically or not. The proportion of plant species in each category differed between the two viruses. Four decades later, Zaitlin and Hull (1987) described resistance operating at four levels: inhibition of replication, cell-to-cell movement, and systemic infection (long-distance movement), as well as defense responses restricting infection to a limited number of Corresponding author: P. Palukaitis Fax: +44. 1382.568523 E-mail: [email protected] Complete resistance in a plant to virus infection is referred to as immunity (reviewed by Bruening, 2006). In plants that convey immunity to viruses in one genotype of a species but not another, the immunity is usually manifested in preventing virus replication. Usually, this is assessed in isolated, single cells (protoplasts), or multiple leaf cells co-infected by agroinfiltration of DNA expressing viral genomes. If immunity occurs against all biotypes of a pathogen and in all cultivars or accessions of a particular plant species the situation is referred to as non-host resistance. For viruses, this is a largely an unexplored area, although some strides are being made in understanding non-host resistance operating against fungi (reviewed by Ellis, 2006; Bittel and Robatzek, 2007; Hückelhoven, 2007; Wise et al., 2007; Hadwiger, 2008). Some resistance genes have been described as conveying extreme resistance (ER). In some cases these may actually convey immunity, in that no virus multiplication could be detected (Barker and Harrison, 1984; Watanabe et al., 1987) while in the case of Potato virus X (PVX), replication occurred to a limited extent and then an induced resistance occurred, leading to prevention of further replication (Köhm et al., 1993). In cowpea (Vigna unguiculata) cv. Arlington, where a dominant resistance limiting accumulation of Cowpea mosaic virus (CPMV) in protoplasts was described, the resistance was due to inhibition of the polyprotein processing of this virus (Ponz et al., 1988). 001_JPP_Review_153 21-07-2008 9:58 Pagina 154 154 Resistance to viruses Journal of Plant Pathology (2008), 90 (2), 153-171 In those instances where replication of viruses occurred at normal levels, but the virus was prevented from moving outside of the inoculated cells, a subliminal infection was said to occur (Sulzinski and Zaitlin, 1982) and further infection was thought to be inhibited by either a dysfunctional viral-encoded movement protein for that plant genotype or some barrier in that plant genotype that prevented the normal function of the viral movement protein (reviewed by Waigmann et al., 2004; Ueki and Citovsky, 2006). In some cases, specific resistance genes of the plant have been identified in blocking or preventing viral cell-to-cell movement, with corresponding changes occurring in mutants of those viruses that can overcome the resistance gene (reviewed by Kang et al., 2005a; Bruening, 2006). In some plant genotypes the virus can move cell-to-cell to a limited extent, before a multicellular hypersensitive response (HR) occurs, which first activates defense responses preventing the infection from spreading further and then kills the cells within the infected zone (reviewed by Gilliland et al., 2006a; Loebenstein and Akad, 2006). The ER and HR are referred to as types of innate resistance. Both are associated with dominant resistance genes (reviewed by Bruening, 2006; Maule et al., 2007). Plants undergoing an HR also induce a state of pathogen-nonspecific resistance called systemic acquired resistance (SAR) (reviewed by Gilliland et al., 2006a). SAR is activated by defense signalling responses and will be considered below. If no ER or HR occurs, then the virus may continue to spread cell-to-cell throughout the leaf, as well as into and within the vasculature. If the virus cannot spread to upper leaves of the plant, then it is likely that there is a barrier to infection preventing the virus from ingressing into the sieve elements of the phloem (Waigmann et al., 2004; Bruening, 2006; Ueki and Citovsky, 2006). This barrier may prevent movement into one or more of the cell types within the vasculature: bundle sheath cells, vascular or phloem parenchyma cells, and/or companion cells. Ingress into the sieve element from the companion cells also may be blocked, as might egress from the sieve elements to companion cells, and then to other vascular cells, although data from grafting experiments tend to suggest that ingress rather than egress is the major barrier (Bruening, 2006). The above observations are consistent with the work of Holmes (1946) on the extent of virus infection in 310 species of plants infected by TMV vs. TEV (Table 1). He showed that infectivity could not be recovered from the inoculated leaves by back inoculation to a susceptible host from 111 of 310 plant species inoculated with TMV and 227 of 310 plant species inoculated with TEV; i.e., they were immune or possibly had a subliminal infection. On the other hand, infectivity could be recovered from the inoculated leaves, but not from the upper leaves of 127 (TMV) and 22 (TEV) inoculated plant species, while infectivity could be recovered from all leaves of 72 (TMV) and 61 (TEV) inoculated plant species. Infection of upper leaves may be limited to a few leaves, before the plant recovers. This may be a manifestation of age-related resistance, which appears to be a salicylic acid (SA)-mediated form of innate resistance (Garcia-Ruiz and Murphy, 2001), or may be due to the inability of the virus to completely block RNAi (Ji and Ding, 2001). Most viruses probably encode RNA silencing suppressors, which prevent one or more steps associated with RNAi (Li and Ding, 2006). In plants showing recovery from infection by nepoviruses and tobraviruses, recovery is due to a failure of the virus to prevent RNAi from being established ahead of the virus infection in upper, newly formed leaves (Ratcliff et al., 1997, 1999). This recovery from infection also occurs in some hosts after infection by Cauliflower mosaic virus (CaMV) (Covey et al., 1997). Tolerance is a manifestation of resistance in which the plants may show only mild or no symptoms as a function of infection (Bruening, 2006). In the experiments described by Holmes (1946), virus also could be Table 1. Susceptibility types to Tobacco mosaic virus (TMV) and Tobacco etch virus (TEV) in 310 plant species tested. Plant response No symptoms No recovered virus No symptoms Virus in inoculated leaves only Local symptoms Virus in inoculated leaves only No symptoms Virus in upper leaves Systemic symptoms Virus in inoculated leaves Inoculation with TMV No. of species 111 100 27 15 57 Inoculation with TEV No. of species 227 15 7 8 53 2007). thaliana. 2006. Recessive resistance. Using a candidate gene approach. A list of the virus resistance genes that encode such proteins is shown in Table 2. 2006. The proteins encoded by these resistance genes show considerable similarity in their organization. a nucleotide binding domain (NB). recessive genes are involved (reviewed by Fraser. Kang et al. Most of the resistance genes isolated are dominant genetically and are involved in resistances manifested by an HR or an ER (Maule et al. insects and nematodes (Jones and Dangl. 2006). while resistances to the bymoviruses and MNSV are associated with eIF4E only. Meshi et al. 2005). 1982. 153-171 Palukaitis and Carr 155 recovered from various leaves of different plant species.. 1988. 2000). while the allele for susceptibility does not have such a role. 1980. In addition... Most of these resistance genes have not been isolated and so remain uncharacterized. more than 20 resistance genes have been isolated and characterized (Maule et al. The relationship between recovery and tolerance has not been investigated in detail. in most cases examined. 2002. RESISTANCE GENES Many resistance genes have been described operating against specific viruses in particular crop species (reviewed by Fraser. 1977. Bruun-Rasmussen et al. 2004. the carmovirus Melon necrotic spot virus (MNSV) (Nieto et al.. and a leucine-rich repeat (LRR) domain. these proteins presumably function in preventing long-distance movement of TEV in A. 1980) and the Sw-5 gene conferring resistance to Tomato spotted wilt virus (TSWV) (Aramburu and Martí. 1972. but contains a TIM barrel structure identified in a wide variety of enzymes (Ishibashi et al. Stein et al. 2000). 2003. By contrast.. while the RTM2 gene was shown to encode a 41 kDa protein similar to small heat-shock proteins. and the sobemovirus Rice yellow mottle virus (RYMV) (Albar et al. 2005a. 2000). Maule et al.. 1993). 2007)... 2007)... 2005a. Ciuffo et al. 2003. the last of which was not characterized. 1987. Bruening. 2006). 2007).. a recessive resistance gene is thought to be one where the encoded protein is unable to function to promote virus infection. They are all considered to be involved in activating defense signalling responses. Nicaise et al.. Where genes conferring tolerance have been delimited. 90 (2). There is a general assumption that a dominant resistance gene reflects an encoded positive effect limiting or blocking a virus. Hall. multiple....001_JPP_Review_153 21-07-2008 9:58 Pagina 155 Journal of Plant Pathology (2008).. 2006). 2007). Nevertheless. Dominant resistance. tolerance is usually associated with a reduced titer of virus in the plants.. 2005. fungi. Many more resistance genes operate as quantitative traits loci and thus function additively in conferring resistance (Maule et al. 2005). 2007). 2005. for which resistancebreaking strains have been isolated (Pelham. The encoded protein. Gao et al. Bruening. Kang et al. several laboratories have isolated recessive resistance genes (Table 2) conferring resistance against particular potyviruses (Ruffel et al. These resistance genes all encode translation factors involved in the formation of the 40S ribosome complex required to initiate translation of RNAs (reviewed by Robaglia and Caranta. is unrelated to any protein with a known function. Therefore. The resistance to various potyviruses is associated with the translation initiation factors eIF4E and eIF(iso)4E. 2001). tolerance specified by two or three specific genes against Cucumber mosaic virus (CMV) in cucumber could be overcome by co-infection with Zucchini yellow mosaic virus (ZYMV). 2001. while its dominant allele conveying susceptibility can do so. and resistance to RYMV is associated with the trans- . in the past 15 years. in which three functional domains have been defined: an N-terminal domain similar to either a Toll/interleukin-1 receptor (TIR) domain or a coiled-coiled (CC) protein domain. The RTM1 gene was shown to encode a protein similar to the lectin jacalin (Chisholm et al. although in one instance. Watanabe et al.. 1990. Both the RTM1 and RTM2 genes were expressed exclusively in phloem-associated cells and the corresponding proteins localized to sieve elements (Chisholm et al.. 1987.. The Tm-1 gene product was found to block virus replication of both TMV and Tomato mosaic virus (ToMV) in protoplasts (Motoyoshi and Oshima. Kang et al. These include several resistances operating against specific tobamoviruses.. Ishibashi et al. Watanabe et al.. Fraser and Loughlin... 2007). 1980. whether they showed symptoms or not (Table 1).. The resistance of some ecotypes of Arabidopsis thaliana to the systemic movement of TEV requires three genes designated RTM1.. most of them fall into two main groups in terms of common features. 1990. which increased CMV replication in the upper leaves (Wang et al. 2006). while the resistance genes that do not. 2005b. the bymoviruses Barley mild mosaic virus (BMMV) and Barley yellow mosaic virus (BYMV) (Kanyuka et al. by a yet unknown mechanism. 1992. Resistance-breaking strains have also been identified for the Rx gene operating against PVX (Moreira et al. 2006). 1992. These proteins are similar to those associated with resistance to bacteria. Tóbiás et al. Padgett and Beachy. RTM2 and RTM3 (Chisholm et al. although its expression was not stimulated by heat nor did it function in thermotolerance (Whitham et al.. The dominant resistance genes that do not encode such defense signal response activation proteins include the Tm-1 gene from tomato and the genes associated with resistance to systemic infection by TEV in Arabidopsis thaliana. This suggests that tolerance may be a manifestation of RNAi operating against a specific virus. designated p80GCR237. 2004). appear quite different from the rest in form and presumably function. 2006... Resistance genes Dominant genes N Rx1 Rx2 Sw-5 HRT RCY1 Y-1 Tm-2 Rsv1 Tm-2 RT4-4 RTM1 RTM2 Tm-1 PvVTT1 Recessive genes pvr1/pvr2 mol1/mol2 sbm1 rym4/5 pot-1 rymv1 nsv pvr2 + pvr6 C.. tuberosum S. 2007.. 2000 Cooley et al.. 2006 Chisholm et al. A number of A. 2005 Albar et al. melo C. TMV SMV ToMV. 2000 Brommonschenkel et al. 2002 Lanfermeijer et al. 2002 Vidal et al. Cloned genes conferring resistance to viruses. BaYMV PVY. Bean yellow mosaic virus (BYMV). lycopersicum P. TMV CMV TEV TEV TMV. thaliana A. thaliana S. Tobacco etch virus (TEV). 2005. 2000 Takahashi et al. The eIF4E translation initiation factor has been shown to interact with the VPg of several potyviruses viruses while the allelic mutants conveying resistance usually. lycopersicum G. sativa C. Rice yellow mottle virus (RYMV).. annuum PVY. Turnip crinkle virus (TCV). ToMV BDMV Whitham et al. thaliana were identified as being due to changes in eIF4E and eIF4G (reviewed by Robaglia and Caranta. Stein et al... Beauchemin et al. Groundnut ringspot virus (GRSV).... TEV RYMV MNSV PVY. 2006 PSbMV. lycopersicum A.. 1994 Bendahmane et al. Barley yellow mosaic virus (BaYMV). BYMV BaMMV.. max S. annuum L. vulgaris A. GRSV TCV CMV PVY ToMV. 2008). Bean dwarf mosaic virus (BDMV). Cucumber mosaic virus (CMV). vulgaris TMV. lation initiation factor eIF(iso)4G. Charron et al. 2000 Whitham et al. Soybean mosaic virus (SMV). Yeam et al. Melon necrotic spot virus (MNSV). TEV LMV 2 Journal of Plant Pathology (2008).. 153-171 Plant species Virus targets Reference N. Tomato spotted wilt virus (TSWV). Pepper veinal mottle virus (PVMV). 2007. failed to interact (Kang et al. 2003 Gao et al. 2006). but not always. thaliana S. 2005b Nicaise et al.. while mutants conveying recessive resistance to CMV in A. Lettuce mosaic virus (LMV). 2007 Ruffel et al. 2004 Lasfermeijer et al.... sativum H. 2005 Ruffel et al. TEV (a) Virus names: Barley mild mosaic virus (BaMMV). 1999 Bendahmane et al.. thaliana mutants that showed resistance to potyviruses also were associated with changes to eIF4E and eIF(iso)4E. 2007 Kanyuka et al. 2005 Seo et al.. Bruun-Rasmussen et al. 2004. 2006 Ruffel et al. 2006 Nieto et al. 2005b. Michon et al. Tomato mosaic virus (ToMV). 90 (2). Tobacco mosaic virus (TMV). lycopersicum P.. Potato virus X (PVX). tuberosum S.. vulgare S. sativa P. Tomato chlorotic spot virus (TCSV). tabacum S.. tuberosum S. ToMV a PVX PVX TSWV. Potato virus Y (PVY). Pea seed-borne mosaic virus (PSbMV). ..001_JPP_Review_153 21-07-2008 9:58 Pagina 156 156 Resistance to viruses Table 2... 2003 Hayes et al. 2002. thaliana A.. 2000 Ishibashi et al... lycopersicum O... TCSV. Kang et al. 2007 Seo et al. 1990.. non-infected plants (Shulaev et al.. Whitham et al.001_JPP_Review_153 21-07-2008 9:58 Pagina 157 Journal of Plant Pathology (2008). 2006.. 1997). 1992. van Loon and van Strien. Carr. The relationship between SA and signalling mediated by JA and its volatile ester methyljasmonic acid is intriguing... However. However. systemic. Darby et al. 2000) cast doubt on the idea that SA is necessarily an essential translocated signal in SAR induction. Jasmonic acid and ethylene. 2004). 1990. JA is an oxygenated fatty acid (oxylipin) that is a signal in resistance to certain bacterial and fungal pathogens and against insect pests (Reymond and Farmer. Consequently. 1990.. Although SA is needed for the maintenance of basal resistance. 2005) and tobacco (A. or if SA production is decreased by mutation of SA biosynthetic genes (Nawrath and Métraux. Murphy and Carr 2002).. elevation in SA levels in the host. 2002).M.. 2001). thaliana (Ton et al. Because of the counter-defensive action of the CMV 2b protein. 2003).. it appears that ISR is not effective against virus . SAG represents a storage form of SA from which free. JA also regulates a systemic resistance pathway inducible by non-pathogenic microbes [‘induced systemic resistance’ (ISR)] that primes resistance to fungi and bacteria in A.. Huang et al. the isolation of the A. Ji and Ding 2001. will inhibit the systemic movement of the virus (Naylor et al. Mayers et al. Wildermuth et al.. 2006). but are often used as markers of SAR. Truman et al. Murphy and J.. SA is required for the expression of a group of proteins that collectively are referred to as pathogenesis-related (PR) proteins (reviewed by Murphy et al. Hennig et al. Taken together these studies provided evidence suggesting that Me-SA is an important long-distance signal in the induction of SAR following a HR. 1993. unpublished data).. 1997). 1990. Together with the gaseous plant hormone ethylene (ethene).. defective in a gene encoding a lipid transfer protein. SABP2 is an es- terase that can convert methyl salicylic acid (Me-SA) into SA (Kumar et al. However. SA-responsive gene expression has been observed in A.) (Malamy et al. The induction of SAR and. Nobuta et al.. 2003). 2007). 1997). results. Gaffney et al. work from the Klessig laboratory showed that transgenic plants silenced for the gene encoding a SA-binding (SABP2) were compromised in gene expression of PR proteins and SAR induction (Park et al. Dean and Mills. 2005) and increased SA accumulation was observed in potato (Krecic-Stres et al. successful pathogen localization during the HR and the establishment of SAR. biologically active SA can be released in response to further infection (Hennig et al. 1999. It remains to be seen how the induction of what is nominally a defensive response can benefit CMV.. 2004). The ones described from tobacco do not appear to have any role in resistance to viruses. 1993). It has been suggested that in SAR-expressing tissues. During virus-induced HR lesion development. 1999).P.. These results appear to be paradoxical... 1994.. possibly jasmonic acid (JA). Recently. However.. thaliana (Whitham et al.. Ji and Ding 2001.. could be the translocated SAR-inducing signal (Maldonado et al. Thaler et al... 1998. an increase in its biosynthesis can occur during a compatible interaction with certain virulent pathogens. in the case of CMV. With respect to virus infection. 153-171 DEFENSIVE SIGNALLING PATHWAYS IN RESISTANCE Palukaitis and Carr 157 The occurrence of salicylic acid and its derivatives. Me-SA is produced in tissues undergoing an HR (Shulaev et al. 2007). SA (2-hydroxybenzoic acid) plays a central role in the signal transduction pathway that results in SAR and it is required for localization of viral and other pathogens during the HR (reviewed by Alvarez. elicitation of SA biosynthesis by CMV infection is a slow process that is only apparent after systemic movement of the virus to all parts of the plant has already occurred (Ji and Ding 2001. 90 (2). sometimes conflicting with each other. It is a volatile chemical that can diffuse into the air and even induce SAR in nearby. Huang et al... during incompatible and compatible interactions with viruses. Mur et al. consistent with a role in the spread of SAR induction to all parts of the plant. non-necrotizing infections do not normally trigger biosynthesis of SA and the consequent induction of SA-responsive genes (PR genes etc. 1993. during systemic infections with CMV and potyviruses [Turnip mosaic virus (TuMV) in A... maintenance of basal resistance to pathogen infection depends on SA-mediated signalling.. SAG) that accumulates within cell vacuoles (Enyedi et al. Rasmussen et al. 1998. Subsequently. SA can be detected in phloem sap (Métraux et al. obtained from grafting experiments with different nahG-transgenic tobacco lines (Vernooij et al.. plants are not able to express SAR and are super-susceptible to both virulent and avirulent pathogens. 2007. thaliana and Potato virus Y (PVY) in potato]. due to treatment with exogenous SA or induction of endogenous SA biosynthesis by an avirulent pathogen prior to infection with CMV. 2003. based on studies with Turnip crinkle virus (TCV). continued replication or local movement of CMV in systemically infected tissues of the plant will be unaffected by increased SA levels (Naylor et al. 2007). 1995). 2005) (see below). 1999. Métraux et al. Strawn et al. thaliana dir1 mutant. suggested that a lipid or lipid-derived substance. For example.. Whitham et al. 2002. 1998. Most of the SA produced is converted to a glucose conjugate (SA-2-O-β-D-glucoside. to some extent.. 2000). SA biosynthesis occurs initially in and around the developing lesions. but later throughout the entire plant (Malamy et al. if SA accumulation is inhibited by engineering plants to express the salicylate-degrading enzyme SA hydroxylase (nahGtransgenic plants. 2008).. The cytoplasmic domains of the NADPH oxidase proteins have ‘EF-hand’ motifs. Firstly. pioneering transcript profiling work revealed significant positive as well as negative cross-talk between the two pathways (Schenk et al. 2007. thaliana. nitric oxide and protein kinase activation. or by CaMV gene products (Love et al. but from the signalling point of view... thaliana.. 1999. 2006). although since its biosynthesis from 1-aminocyclopropane-1-carboxylic acid results in the release of cyanide (Siegien and Bogatek. In A. PR proteins) versus JA-induced antimicrobial gene products (e. the oxidative burst activates Ca2+ ion influx across the plasma membrane via cyclic nucleotide-gated channels. Reactive oxygen species (ROS) have long been recognized as signals in defense. However.. This permits changes in Ca2+ flux to function both upstream and downstream of ROS production. between the pathways and the ‘choice’ made between expression of SA-induced. suggests that certain viral gene products can function as MAMPS. 2001).. and a recent study suggests that JA plays a role in SAR induction. 2005.. 2005). 2000). leading to the identification of factors such as bacterial flagellin. it is conceivable that this may contribute to the induction of resistance to viruses via the mitochondrial signalling pathway (se below). two members of this family. Ma and Berkowitz.g.and JAmediated signalling pathways are provided by antagonistic effects on the re-localization of WRKY transcription factors from the cytoplasm to the nucleus (Balbi and Devoto. ethylene does not appear to be essential for the induction of resistance to viruses. 1998).or pathogen-associated molecular patterns (MAMPS or PAMPS. which trigger basal or innate immunity (GomezGomez and Boller. Balbi and Devoto. In A. 2007). van Verk et al. Reactive oxygen species. Ethylene-dependent signalling is indispensable for the maintenance of basal resistance to fungi and bacteria (van Loon and van Strien. 1999.. there are ten NADPH genes. Additional points for cross-talk between SA. 2007. Geraats et al. resulting in a positive feedback on ROS production and. the burst is biphasic. In a gene-for-gene interaction. A second effect of alterations in Ca2+ ion concentra- . in concert with nitric oxide (NO). in addition to mobilization of Ca2+ ions from intracellular stores (Torres and Dangl... of which two (AtrbohD and F) encode enzymes that function during the HR. 2000). the rest play roles in other plant functions such as development (Foreman et al. ROS have several roles during the HR. 2006 and references therein). 2000. NADPH oxidase catalyses the formation of superoxide (O2-) anions that are readily converted to other ROS. most notably during the oxidative burst or bursts that occur very early in the HR during a gene-forgene response (Heath. defensins) is regulated at several levels. characteristic of proteins regulated by Ca2+ ion levels (Keller et al. respectively) in basal resistance (see Mackey and McFall. or ‘cross-talk’. However. 2007). 2007). thaliana.g. 2007). 2002). The oxidative burst. with an initial small burst (probably wound. 90 (2). followed later by a sustained burst that is often associated with the onset of host cell death (reviewed by Torres and Dangl.HO2) and hydrogen peroxide (H2O2). Li et al.. Miao and Zentgraf. 2000) or during recognition of microbe. 2006) (see next section). amino acid sequences within the coat proteins of potexviruses (Baurès et al.. thaliana (Love et al.. helping to drive cell death in the HR (see below). 2003).. Various members of this large family of transcription factors (characterized by the amino acid sequence motif WRKYGQ/KK) are up-regulated during defense responses mediated by both SA and JA and the promoters of many defense-related inducible genes (including PR genes) contain ‘W-boxes’ for WRKY binding (Du and Chen. 2008). It has been proposed that this may explain a de- crease in susceptibility to infection with CaMV observed by Milner and colleagues in the ethylene signalling mutant etr1 in A. MAMPS have been investigated most extensively in studies of basal resistance to bacterial pathogens. Other work has shown that JA is synthesized transiently in the earliest stages of a TMVinduced HR and may play a minor role in localization (Kenton et al. the products of the PAD4 and EDS1 genes promote SAmediated gene induction and repress gene expression induced by JA. Ethylene is produced copiously during the HR and is a strong inducer of certain PR genes. calcium signaling. Liu et al. In A. which until recently was considered a JA-independent process (Truman et al. These regulatory proteins are themselves negatively regulated through phosphorylation catalyzed by a protein kinase (Brodersen et al. which occurs in cells in the immediate vicinity of the infection site. 2004). is due predominantly to the activation of NADPH oxidase associated with the plasma membrane. 2007.with JA-mediated signalling and that regulate the responses of these pathways to either pathogen attack or the developmental and environmental cues that trigger senescence (Balbi and Devoto.or MAMP-induced). The interplay. 2007). Although the JA and SA pathways are viewed predominantly as being mutually antagonistic. anti-microbial gene products (e. including the perhydroxyl radical (. perhaps two are the most important. 153-171 infection (Ton et al. It is also possible that ethylene plays a role as a negative regulator of SA-mediated resistance to viruses.001_JPP_Review_153 21-07-2008 9:58 Pagina 158 158 Resistance to viruses Journal of Plant Pathology (2008).. 1997). 2004).. the triggering of transient or even sustained ROS and ethylene production by TMV coat protein (Allan et al. WRKY53 and WRKY70 appear to act as crucial nodes in a network that maintains the equilibrium between SA. via non-enzymatic and enzymatic mechanisms (Lamb and Dixon.. 2005) in susceptible hosts. 2007. 2004). 2000. Thus. in part by inducing the biosynthesis of SA (Song and Goodman. SIPK and an upstream MAPKK are needed for full N gene-mediated resistance to TMV. 2000. However. Nevertheless. thaliana.. PR gene induction and establishment of induced resistance (Pedley and Martin. 2008). Chen and Chen. the available data on the mechanism(s) of NO production in plants are confusing (reviewed by Hong et al. For example. There also exists uncertainty about the nature of the PCD that occurs during the HR.and SA-induced protein kinases (WIPK and SIPK.. increased expression of genes for TGA. Jin et al. The process has sometimes been described as a variant of apoptosis. such as DNA . at present. This mode of action may prove to be more important directly in resistance to viruses (see below). 2008). no specific substrates have been identified. knockout of the gene for MAPK4 results in constitutive expression of genes controlled by the SA-regulated pathway and knockout of responses to treatment with JA (Brodersen et al. 153-171 Palukaitis and Carr 159 tions in the cytoplasm is triggering of the activity of calcium-dependent protein kinases.. 2008). 2003. 2008). there is no evidence that the PR proteins are involved in virus resistance (reviewed by Murphy et al. it is not always clear how they control defense. NO may exert some of its effects via modulation of cyclic nucleotide-based signalling (Wendehenne et al. an animal PCD effector protein. With respect to a role in resistance to viruses for MAPK cascades. there is no evidence that plant genomes encode either orthologues of animal caspases or Bax-type proteins. NO regulates defense gene expression both at the point of infection and in distal tissues. 2006). 2001. suggesting that new classes of defense gene await identification (Liu et al. Zhang and Klessig. there are a few examples in which their roles have been revealed. The relative tissue levels of NO and H2O2 appear to regulate programmed cell death during an HR (Delledone et al.. 2006). Liu et al. silencing of expression of specific WRKY and Myb factors in tobacco did decrease the efficiency of N gene mediated resistance to TMV. SIPK. several studies using over-expression or virus-induced gene silencing of candidate genes in either tobacco or N. although MAPK cascades have been studied intensively. Thus. MAPKK kinases (MAPKKKs). we still do not understand its significance in resistance – particularly with respect to viruses (Mur et al. 1998).. and so on (Ma and Berkowitz. caspases are aspartate-specific cysteine proteases that are important effectors of apoptosis in animal cells and several groups have reported increased cysteine protease activity during the HR (reviewed by Birch et al. In tobacco and pepper. 1999). van Verk et al. as well as highly complex mitogen-activated protein kinase (MAPK) cascades. Lam and del Pozo. the equivalent (orthologue) to the tobacco SIPK (Liu and Zhang. 2002). NO is an important defensive signal and probably exerts a positive feedback on Ca2+ flux by enhancing calcium release from endomembrane stores (Ma and Berkowitz. though inaccurately. MAPK4 is an important regulator of the ‘antagonism’ between SA... The connection between these factors and virus resistance is unclear. it is clear that MAPK cascades play roles in tissues within and beyond the infection site and participate in the control of cell death. Although members of the transcription factor families are known to be involved in the induction of PR gene expression. only one in vivo substrate with a clear role in defense has been identified: the ethylene biosynthetic enzyme 1aminocyclopropane-1-carboxylate synthase. but not WIPK. However. 2002). 2004. Nevertheless.. is required for cell death induction during the HR. From studies in a variety of plant species.. In many cases.. 1999). Although hypersensitive cell death has been studied scientifically for almost a century. MAPK cascades function in plant defense responses and probably the best studied of these are the wound. induced PCD when expressed from a viral vector (Lacomme and Santa Cruz. especially with respect to defense against viral pathogens. 2000). thaliana is the substrate for MAPK6. Calcium flux regulates biosynthesis of NO in animal cells and is thought likely to be a strong influence on NO production during plant defense responses. 1996. Hong et al. Liu et al. 2001). 90 (2). Myb and WRKY transcription factors occurred after a TMV-induced HR or following treatment with SA (Yang and Klessig. Park et al. the phosphorylation targets for defense-related MAPKs are likely to be transcription factors. 2001).. while other characteristics of apoptosis. WIPK. In A. However.. Nevertheless.. Furthermore. However. Cell death and the hypersensitive response... Programmed host cell death (PCD) accompanies many gene-for-gene interactions and the term ‘HR’ is used often.and JA-mediated defensive signalling (see above). to describe this correlative feature of resistance. Although proteomic studies have revealed likely substrates for MAPKs (Merkouropoulos et al. 2004) and by the S-nitrosylation of protein targets (Hong et al. 2006). 2004). 2008). 2008). which in A. 2004). benthamiana plants expressing a transgene for the N resistance gene indicate that MAPK activity is required for TMV localization in the HR (reviewed by Caplan and Dinesh-Kumar. NO also may stimulate changes in nuclear gene expression and defensive signalling indirectly through inhibition of cytochrome oxidase (Huang et al. The identities and functions of the protein substrates for defense-related MAPKs remain elusive.001_JPP_Review_153 21-07-2008 9:58 Pagina 159 Journal of Plant Pathology (2008).. This process can lead to changes in mitochondrial redox and the induction of specific sets of defense related genes (Maxwell et al... indicating a branch in the MAPK-mediated signalling pathway (Yang et al. 2006).. MAPKs are activated through phosphorylation by MAPK kinases (MAPKKs) that are in turn activated by upstream protein kinases. 2006. regulation of ROS production. Bax. 2006). and more recently. 2004). Mur et al. Only when the coat protein was expressed using agroinfiltration in large swathes of leaf tissues in Rx-containing potato plants was HR-associated cell death induced (Bendahmane et al.. Santa Cruz and colleagues (Wright et al. Consistent with this idea. Thus... suggested that these proteins may have the capability of acting on the promoter of the gene for the ethylene biosynthetic enzyme 1-aminocyclopropane-1-carboxylic acid synthase (Matarasso et al. a study of HR-type resistance to CMV in cowpea showed that specific and distinct amino acids within the viral RNA polymerase sequence were responsible for the induction of virus localization and the elicitation of cell death (Kim and Palukaitis. 2008). 2007). thaliana VPE (VPEγ) was enhanced during a compatible infection with TuMV in which no HR-type necrosis occurred (Rojo et al. cell death in the HR involves breakdown and re-cycling of cellular materials. Although host cell death is a prominent feature of N gene-mediated resistance to TMV. . from the point of view of plant-virus interactions. does not normally elicit cell death and appears to be an extreme form of resistance (ER... 90 (2). An inhibitory peptide synthesized to mimic this cleavage site retarded the appearance of HR-associated cell death in the TMV:N gene interaction (Chichkova et al. Mittler et al. expression of the A. This enzyme cleaves only a single bond in a model substrate for caspase (the virD2 protein of Agrobacterium tumefaciens) while human caspase cleaves at two sites. vacuolar processing enzymes (VPEs) with caspase-like activity have been reported in Nicotiana spp. Interestingly. (2008) applied antioxidant agents to inhibit TMV-induced ROS generation. Király et al.. see above). the gene-for-gene resistance to PVX. How an apparently vacuolar localized protein influences the activity of nuclear DNA is puzzling. it did not prevent localization of TMV in NN genotype tobacco (Chichkova et al. plant metacaspases. Studies in other systems have shown that cell death is either not required for resistance or can be separated from resistance on a genetic basis (Schoelz et al. Weststeijn (1981) exploited the temperature-sensitive nature of necrotic lesion formation and TMV localization in tobacco containing the N resistance gene to show that increased temperature could facilitate the escape of virus from lesions for up to 12 days following the first appearance of TMV-induced lesions. Work with a cysteine protease from tomato. Perhaps the nearest functional analog of a caspase found to be associated with the HR was discovered by Chichkova and colleagues (2004). jasmonate-regulated F-box protein in tobacco inhibited N gene associated cell death but did not inhibit N gene mediated restriction of TMV infection (van den Burg et al. Matarasso and colleagues (2005) proposed that a posttranslational modification of tomato VPE allowed a proportion of the protein synthesized to migrate to the nucleus. (2003). are not clearly apparent during the HR (Mur et al. who showed increased expression of SA-inducible genes by this virus. Additionally.. 153-171 laddering. Cell death and resistance can be induced by separate domains within a single viral elicitor molecule. 2004).. given the likely role of the vacuole and related structures in the autophagy.. Rojo et al. 2001). thaliana. 2004).. Significantly.. rather than their outright destruction.001_JPP_Review_153 21-07-2008 9:58 Pagina 160 160 Resistance to viruses Journal of Plant Pathology (2008).. thaliana) or small lysosomes (in tobacco). Thus. 2007). Taken together with the observations of Whitham et al. Consistent with the idea that cell death and resistance are separate processes it was observed during the study of a caspase-like activity in tobacco that while pharmacological inhibition of its activity slowed the cell death process. and A. The process of autophagy involves the compartmentalization of cytoplasmic material into double-membrane bound vesicles (autophagosomes) that fuse with either the vacuole (in A.. (1996) grew NN genotype tobacco plants in an oxygen depleted atmosphere to inhibit ROS formation and cell death following inoculation with TMV. 2008). silencing of a newly discovered HRinduced. 2004. 2005. 2000) used genetically engineered TMV expressing green fluorescent protein to confirm that virus remained in living cells at the periphery of the HR lesion for several days following the appearance of the HR in NN genotype Nicotiana edwardsonii. Recent work with the N gene-mediated HR in tobacco suggests that defensive PCD is a form of autophagy (Liu et al. In both studies plants were still able to inhibit the spread of the virus. and appear to contribute both to cell death during the HR and to inhibition of pathogen spread (Hatsugai et al. where degradation occurs (Bassham. In other words.. Similarly. 2008). There is no direct evidence from any system showing that cell death is an absolute requirement for the limitation of virus spread during an HR. 2004).. which are similar in several respects to animal caspases. this suggests that VPE γ expression is stimulated by SA and may be part of a delayed resistance response. conditioned by the Rx gene and the viral coat protein. in potato. Furthermore. 2004). 1999). In other systems autophagy is used to remove defective structures or as a means of rapidly providing intermediates for energy generation (reviewed by Bassham. several studies indicate that it is dispensable. confirming that cell death induction and virus localization are separate processes. knockout of VPE gene expression causes a modest increase in the accumulation of TuMV (Rojo et al. do not cleave caspase substrates and it is not thought that they are involved in the HR (Bonneau et al. 2005). 2008). 1997). suggesting a greater degree of specificity than its mammalian equivalents. with 94 % similarity to the tobacco VPE.. cell death and resistance induction triggered by CaMV in Nicotiana species are controlled by separate host genes (Cole et al. . the action of which has been studied extensively (reviewed by Nielsen and Boston. 2001). 2003). Huang et al. AOX is encoded by a small family of nuclear genes. 2003). Studies of the potential role of AOX in pathogen resistance led to the discovery that SA-induced resistance to viruses is mediated in part by a pathway that appears to involve signals transduced through changes in redox or ROS in the mitochondria. thaliana (Lacomme and Roby. it cannot be regulated by the same signalling pathway as the PR proteins since its expression is not dependent upon NPR1.. Aox 1a. a ribosome-inactivating protein. and cellular responses to ROS. so far. which connects oxidation of the ubiquinol/ ubiquinone (UQ) pool directly to the reduction of oxygen to water.6-dichloroisonicotinic acid (Rhoads and McIntosh. Evidence for the existence of a mitochondrial signalling pathway regulated by AOX came from studies using transgenic plants or viral vectors to alter alternative pathway capacity (Gilliland et al... AOX is synthesized in the cytoplasm and is posttranslationally translocated into the mitochondrion (Vanlerberghe and McIntosh.. However the work also indicated that SA can activate additional AOX-independent resistance mechanisms against TMV. Murphy et al. 2004).. A. Similar findings with respect to the DNA virus CaMV in A. we have considered ROS as products of the oxidative burst. 2004). replication inhibitors. Alternative Oxidase (AOX) and mitochondrial redox signalling. 1993. The effects of altering alternative pathway capacity on chemically-induced resistance to TMV were . 2002. thaliana. a subset of which are inducible. 1999.. kinases. Moreover. is inducible by chemicals such as cyanide or antimycin A. For example. In addition. excess electrons flowing into the UQ pool are dissipated.. 2002. Huang et al. 1997. Yip and Vanlerberghe.. 1999. Pasqualini et al. 1993).. proteinases. Within mitochondria the respiratory electron transport chain constantly gives rise to ROS as a by-product of its activity (Yip and Vanlerberghe. 1998). 2003.. Although no ATP is generated by the alternative respiratory pathway. Initial evidence for this included observations that resistance to replication and/or movement of CMV. These chemicals probably induce changes in Aox gene expression by inhibition of electron flow through the cytochrome pathway (Xie and Chen. Wong et al. Gilliland et al.. Aox gene expression also increased in tobacco (Lennon et al. including RNAi mediated by RDR1 (Gilliland et al. its activity ensures that respiratory metabolism can continue under conditions of stress (Maxwell et al. which inhibit electron flow through the cytochrome pathway... nuclear gene expression (Maxwell et al... PVX and TMV in tobacco... 2007. These components include various transcription factors (described above) and enzymes involved in various processes. the so-called ‘alternative’ or ‘cyanide-resistant’ pathway. In all plants examined to date. 2001. 2001. 2002). causing an increase in mitochondrial ROS levels (Wong et al. 2002). 1999. thaliana has at least four Aox genes. this pathway is separate from the NPR1-dependent pathway required for SA-induced PR gene expression and resistance to fungi and bacteria (Chivasa et al.. 2006b). 1999.. Murphy et al. Singh et al. Various examples of such factors are described below. Singh et al. 2005... 2004). of which one.. 2001.. This suggested that AOX acts as a negative regulator of induced resistance to viruses (Gilliland et al. 1997. including. the key regulator of SA-induced PR gene expression (Wong et al. 1997). 90 (2). can be induced with non-toxic levels of antimycin A or cyanide (Chivasa and Carr 1998. Among the genes affected in this way are some of those encoding members of the Aox gene family themselves (Norman et al. Although. Increasing the capacity of the alternative pathway to scavenge mitochondrial ROS compromised resistance to TMV induced by antimycin A. 2004). as well as of Turnip vein clearing virus in A. By engaging AOX. 1998) and A. 1999) in tissues undergoing a HR induced by viruses or other pathogens. 2004a). and others that have been reported but not assessed further. 2007). Plant mitochondria can minimize ROS generation while maintaining efficient electron flow into and through the respiratory chain using an enzyme called the alternative oxidase (AOX). ROS are produced at all times as by-products of normal metabolic activity (Noctor and Foyer. 2002. thaliana have been reported (Love et al.. Norman et al. AOX is the sole component of a distinct branch of the respiratory pathway. Nevertheless. and resistance induction by SA or antimycin A was enhanced in transgenic tobacco plants with decreased alternative pathway capacity. In addition to those listed below. strong evidence exists to indicate that the ability of AOX to modulate the levels of ROS in the mitochondrion allows it to regulate ROS-mediated signal transduction and indirectly. 2002.001_JPP_Review_153 21-07-2008 9:58 Pagina 161 Journal of Plant Pathology (2008). 2002. Chivasa and Carr. NO and 2. Increased Aox gene expression and AOX activity is also triggered by natural and synthetic inducers of pathogen resistance such as SA. Chivasa et al. The Aox 1a promoter from tobacco has certain sequence motifs in common with the promoters of genes encoding PR protein (Rhoads and McIntosh. RNases. Park et al. 2002). 153-171 RESISTANCE FACTORS Palukaitis and Carr 161 Achievement of dominant gene-mediated resistance usually involves factors and components at the beginning and at the end of pathways activated by the dominant resistance genes. Moore et al. RNA polymerases. 2002).. Affourtit et al. plants have been shown to produce other antiviral factors that either when added to virus inocula or previously applied to plants can inhibit virus infection to various degrees. Simons et al. Wong et al. 2004). 1999.. These include the pokeweed antiviral protein. 2007). 1983. Pasqualini et al. W. the stimulation of RDR1 gene expression by SA. NtERF5 is also not activated by either SA or JA (Fischer and Dröge-Laser. 2003). These data also suggest that p80GCR237 functions stoichiometrically and not catalytically and therefore can be saturated or lead to resistance breakdown allowing delayed infection to occur with time. in other instances. tabacum (Xie et al. SA-independent mechanism (W. at least not against the viruses tested. In tobacco. p80GCR237. thaliana (Yu et al. 2003) and silencing RDR1 gene expression in A. thaliana genome identified six genes with similarities to the tomato RDR gene (Yu et al. RNA-dependent RNA polymerase (RdRp1). can have dramatic effects on the ability of plants to resist viruses other than TMV (R. ERF5 is a tobacco transcription factor. whereas it was thought that NO induced resistance to TMV via an SA-dependent mechanism (Song and Goodman. but its natural expression was temperature sensitive. 2007). 1986) now designated RdRp1 (reviewed by Wassenegger and Krczal. it now appears that NO can induce resistance rapidly via an additional. with little expression at 32°C. 2006). thus masking regulatory signals and preventing them from functioning in translation or replication. high-level expression of wild-type and mutant AOX proteins from a TMV-derived vector greatly enhanced the susceptibility of N.P.P.. once the replicase complex has been formed. even though NtERF5 gene expression did not respond to ethylene (Fischer and Dröge-Laser. Its exact role in virus infection was not known. 2004).. Tobacco ethylene response factor 5 (NtERF5). although at one time there was speculation that it might be involved in virus infection (Fraenkel-Conrat. NtERF5 gene expression was enhanced by infection with TMV. 2003). benthamiana altered the disease resistance profile after infection by several tobamoviruses tested. Nevertheless. thaliana in sequence and there were four other tobacco ERFs previously identified. Infection of tobacco and numerous other species by viruses had been shown to induce an RNA-dependent RNA polymerase (RdRp) (reviewed by Fraenkel-Conrat. 153-171 subtle. 1998).. N. the role of RdRp1 in virus resistance appears to be limited to specific viruses. and by Tobacco rattle virus (TRV) and TMV-Cg in A. the Tm-1 gene has been shown to provide resistance in the field. and to prevent systemic infection of TMV in tobacco plants expressing the N gene at 32°C. benthamiana was shown to express a translationally defective RDR1 gene. thaliana did not affect RNAi (Yu et al. thaliana by SA (Xie et al. Watanabe et al. so named because it resembled ERF1 from A. Verchot-Lubicz. and therefore represents an independent defense response against TMV from that activated by the SAdependent defense pathway. SA-mediated defense response is inactive against TMV. J. indicating that the RdRp1 was not required for RNAi.. 2003). 2004).. Lee and J. 2000.. Interrogation of the A. Fu. In contrast. unpublished data). However.. 1987). However. in more recent work it has been found that even the relatively small changes in alternative pathway capacity. that binds to the 126 and 183 kDa proteins of both TMV and ToMV and prevents them from assembling into the active replicase complex.. Other recent experiments with Aox-transgenic tobacco indicate that. 1972. However. 2003.. Whether or not RdRp1 functions though a separate RNAi pathway is not clear. thaliana RDR gene shown to be involved in RNAi was designated RDR6. and silencing of tobacco RDR1 did not prevent the SA-mediated resistance from being induced (Xie et al. indicating that RdRp1 was one of several components acting against TMV during the SA-mediated defense response. 2004). thaliana identified a gene in each case resembling the tomato RDR gene (Cogoni and Macino.. with mutations in the viral-encoded 126 kDa protein (Meshi et al. unpublished data). which in fact was described (Fraser and Loughlin.... Yu et al. the tomato gene was designated RDR1 and the A. RDR1 gene expression was stimulated in both tobacco and A.. The Tm-1 gene encodes an 80-kDa protein. 2000).001_JPP_Review_153 21-07-2008 9:58 Pagina 162 162 Resistance to viruses Journal of Plant Pathology (2008). Carr. A cDNA clone of a gene transcript encoding an RdRp (RDR) was isolated from tomato (Schiebel et al. 1988. the 126 and 183 kDa proteins cannot bind to p80GCR237 (Ishibashi et al. Hamamoto et al. Silencing the RDR1 gene was shown to affect infection by TMV and PVX in N.S. 2001). 1983). 2004). Hall. 2001). but not against CMV or PVX (Yang et al. AOXregulated. Carr. 2001. 1980. Thus. Thus... Dalmay et al. benthamiana to virus infection (Murphy et al.. 1997). 2001). Mourrain et al.S. designated p80GCR237. constitutive expression of a Medicago truncatula RDR1 orthologue of NtRDR1 in transgenic N. 1999. 1980).. Transgenic over-expression of NtERF5 was found to reduce TMV accumulation in the inoculated leaves. Liang and J. Work on defining genes involved in RNAi in Neurospora crassa and A. RdRp1 does not require primers for complementary RNA synthesis (Fraenkel-Conrat. 2004). 2003). The success of this resistance gene may reflect the fact that the 126 kDa protein is also the RNA silencing suppressor of ToMV and TMV and is involved in virus movement and activation of defense responses . when the N gene. The inhibitor of TMV replication. 1986) and may function by making regions of single-stranded viral RNA templates double-stranded. although resistance-breaking strains have been identified (Pelham. which was thought to explain the susceptibility of this host to many viruses (Yang et al. 90 (2). independent of the AOX pathway (Gilliland et al. which can be produced by constitutive expression of Aox-derived transgenes in tobacco (Gilliland et al. based on phylogenetic analysis.. both of which were found to be induced during an incompatible reaction between TMV-P0 and C. 1983). Interestingly. also known as paraquat). 2003). ethylene. the RNase PR10 present in roots was also a mixture of phosphorylated and non-phosphorylated protein. and MV (Shin et al. gave enhanced resistance to TMV. annuum cv. 2000. debneyi (Loebenstein et al. 2005) or naturally in a hybrid Nicotiana derived from a cross between N. CaTin2 also was induced by treatment with SA.. It is not known by what pathway transcription of the tobacco IVR gene is induced. as well as to a lesser extent in flowers. The mode of action of IVR is not clear.. TMV-induced gene (CaTin2) encodes a mature 23 kDa protein that contains little sequence similarity to other cell wall proteins. the purified proteins did not resemble interferon in sequence (Edelbaum et al. 2004b).. CaPR-10 was shown to be an 18 kDa RNase with no apparent sequence specificity.. 1990). 2004). CaTin2 was expressed preferentially in leaves and roots. 1981). 2002. the encoded protein was phosphorylated.. led to inhibition of virus accumulation (Sela and Appelbaum. AVF is a family of phosphorylated glycoproteins stimulated in TMV-infected N-gene tobacco that when mixed with TMV. CONCLUDING REMARKS Since the initial experiments done by Holmes (1946) demonstrating different levels of resistance to two viruses. between one and two weeks after inoculation. but not during a compatible reaction between TMV-P1.. Both AVF and human β-interferon stimulated plants to produce nucleotides with antiviral activity (Reichman et al. appeared to be a β-1. 2007). Sela. CaPR-10 transcription was induced by SA. although it was not stimulated by exogenously applied SA (M.. 2004). Grube et al. JA. Transcription of the gene encoding PR-10 (CaPR-10) was induced in leaves during the incompatible response elicited by TMV-P0. A protein induced by TMV infection in N gene tobacco was isolated and was found to inhibit the accumulation of TMV (reviewed by Loebenstein and Akad. In addition... and more slowly by ABA. During induction of CaPR-10 in leaves. Although IVR was induced by the N gene-mediated response against TMV. Genda et al. constitutive expression of CaTin2 in transgenic tobacco resulted in some resistance against TMV or CMV.. Pathotypes of the tobamoviruses TMV and Pepper mild mottle virus (PMMV) can break resistance conferred by specific L genes (Alonso et al. CaPR-10 was expressed constitutively in roots and was not upregulated by infection with TMV0.. and in common with other cell wall proteins.. 1962. capable of degrading both TMV RNA and plant RNA... resistance to several tobamoviruses is controlled by the allelic genes L1-L4 (reviewed by Grube et al. Bugang carrying the L2 resistance gene (Shin et al. IVR applied to leaf discs or leaves could inhibit accumulation of CMV.. 1991). PVX or PVY (Gera and Loebenstein.. Whether it also can interfere with subsequent steps in virus infection is not know. 1981). 1983). Ding et al. ethylene. However.. which increased its specific activity. 2003. glutinosa x N. This suggested that the expression of the CaTin2 cell wall protein probably was limiting virus movement and accumulation. 90 (2). although the resistance was lost by one month after inoculation. which generates superoxide radicals (Park et al. By contrast. but not by the compatible response elicited by TMV-P1. Takeshita and P. 2004b). IVR probably is not a transcription factor. IVR does not have singlestranded RNase activity (Gera and Loebenstein. Park et al. several factors have been identified that may play key roles in resistance to tobamoviruses in Cap- sicum spp. 2000. AVF was purified using antibodies to human β-interferon. Tsuda et al. 153-171 Palukaitis and Carr 163 (Kubota et al.. JA. 2006). Hamada et al. Since it accumulates in the intercellular spaces (Spiegel et al. considerable progress has been made in understanding the nature of resistance and in isolating resistance . Thus. a reduced availability of the 126 kDa protein may have more than one effect on virus accumulation. 1983). Tobacco inhibitor of virus replication (IVR). 1989). however. These include PR-10 and the Tin2 gene product. although whether it has double-stranded RNase activity has not been evaluated. In Capsicum spp. Palukaitis.2 and hot pepper carrying the L2 resistance gene. Sawada et al. but not detectably in stems or fruit. it apparently interferes with virus replication (Loebenstein and Gera. CaTin2 was induced during the incompatible response elicited by TMV-P0. 2003.. The two purified glycoproteins. but their roles in the defense against virus infection are not known. annuum. 1998. but as it can be applied to protoplasts infected with TMV 4 to 18 h after inoculation and still reduce virus accumulation. 1990.001_JPP_Review_153 21-07-2008 9:58 Pagina 163 Journal of Plant Pathology (2008).. the IVR was not target-specific in its interference. except for the 26amino acid signal peptide. Other pepper genes that appear to be involved in the defense response were shown to be induced during this incompatible response. The C. 1991). Resistance factors induced in Capsicum annuum. sodium chloride and the herbicide methyl viologen (MV. pg35 and gp22. 1991. Tobacco antiviral factor (AVF). either in transgenic tobacco (Akad et al.. 2002) and an alanine aminotransferase (CaAlaAT1) (Kim et al. Constitutive expression of IVR.2. 2005). sodium chloride.3-glucanase and an isoform of PR-5 (Edelbaum et al. unpublished).. such as genes encoding a lipid transfer protein (CaLTP1) (Park et al. prior to inoculation. fluorescently-tagged CaTin2 appeared to localize to the cell wall in cells transiently expressing this fusion protein. This is particularly the case for recessive resistance genes operating against potyviruses. Affourtit C.. This is particularly true with respect to specific blocks in long-distance movement. Teverovsky E. Visualization of the interaction between the precursors of VPg.. in some cases. RavDavid D.. Exploring the molecular nature of alternative oxidase regulation and catalysis.. Plant autophagy-more than a starvation response. de la Cruz A. Control of plant mitochondrial respiration... Culver J. Gidoni D...F. It is also hoped that some progress will be possible in the largely unexplored area of non-host resistance.. Akad A. 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